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Who would have ever believed that just rinsing one's mouth with a sports energy drink and not swallowing but spitting it out would improve endurance performance? Not me, at least not until reading the exciting study of Chambers et al. (2009), which considerably challenges our current understanding of exercise physiology. And the evidence of the mechanisms underlying this unexpected finding is puzzling.

Peak performances in endurance sports are realized by individuals who are able to limit the decrease in speed or power output (i.e. fatigue) while competing. The factors limiting endurance performance of prolonged exercise, i.e. the causes of fatigue, remain incompletely understood. Generally, fatigue is explained in terms of limits to oxygen transport capacity and/or muscle metabolic capacity and/or the development of central and peripheral fatigue. Numerous experiments have established that intramuscular processes are impaired during repeated muscle activation. For example, intact single fibres repeatedly stimulated show a decreased force production intimately related to alterations in Ca2+ handling, which can explain the reduction in muscle force production associated with prolonged exercise in humans under certain conditions (Allen et al. 2008). Although fatigue can develop within muscle fibres, motor unit activity is centrally modulated. Indeed, the descending neural drive from the brain to the exercising muscles determines the strategy in terms of motor unit recruitment and de-recruitment during prolonged exercise, and therefore the force-generating capacity of the muscle (Kayser, 2003). Thus, the development of central fatigue would be set above a safe level via integration of multiple neural and humoral inputs to maintain body homeostasis during repeated or sustained muscle contractions. If the safety margin is threatened, the functional outcome would be a reduced neural drive, leading to decreased muscle activity and thus a lowering of exercise intensity or task failure depending on the details of the task.

In a recent issue of The Journal of Physiology, Chambers et al. (2009) assessed the effect of mouth rinsing with carbohydrate solutions on a cycle time trial of ∼1 h duration. Chambers et al. (2009) used functional magnetic resonance imaging in a second set of experiments to identify brain areas eventually activated by oral carbohydrates. Trained cyclists performed time trials simulated on a cycle ergometer (separated by at least 3 days) in a fasted (> 6 h) state, where they had to complete a fixed workload (corresponding to 1 h at 75% maximal work) when complemented with glucose, maltodextrin or placebo (saccharin) solutions. An artificial sweetener was used to reduce sensory clues between solutions. Subjects were asked every 12.5% of the time trial to rinse the solution in the mouth for ∼10 s but not to swallow anything. Intriguingly, the results showed that a 6.4% carbohydrate solution produced an astonishing improvement of 2–3% as indicated by the average power output, when compared to the placebo solution. This could equate to more than 1 min difference in the longer time trials in the Tour de France. The rate of perceived exertion (RPE) was not different between conditions, which led the authors to suggest that oral exposure to carbohydrate reduces the perception of exertion for a given workload allowing them to increase power output during the time trial. The authors hypothesized that the caloric content detected by ‘unidentified receptors’ might mediate a neural response. Neuroimaging measurements then were performed while the subjects at rest rinsed their mouth in the same manner as they did while cycling, showing that oral carbohydrates acted via supraspinal pathways during exercise. Brain activation was similar with glucose and maltodextrin solutions, and brain regions were activated, including the anterior cingulated cortex (ACC), that were not activated with placebo. Previous reports using hypnosis during cycling exercise have shown that ACC activity is closely related to RPE; ACC blood flow decreased when subjects cycled on a cycle ergometer under hypnosis while perceiving a downhill descent compared to a flat, level grade (Williamson et al. 2001). Furthermore, results from Marcora et al. (2009) show that mental fatigue induced by a cognitive task prior to exercise significantly reduces the time to exhaustion when cycling at a workload corresponding to 80% of peak power output. The alteration in endurance performance was attributed to the higher RPE during exercise performed after induction of mental fatigue: a possible implication of the ACC, although this was not quantified, was suspected (Marcora et al. 2009). The novel findings of Chambers et al. (2009) move us forward. They show, for the first time, that central fatigue development during prolonged exercise may be postponed or attenuated by activating brain regions that were possibly inactive or inhibited. Nevertheless, these results raise several new questions: what are the receptors that convey sensory information from the mouth to the brain? Would the same results have been observed in a competition situation, i.e. in a fed state? Would it be possible to observe improvements in performance in highly trained athletes? Indeed, one can calculate that performance over a half-marathon (∼1 h duration) not realized in the heat would be improved if the athlete does not swallow the solution by preventing (i) any, even minor, weight gain and (ii) risks of gastrointestinal problems, frequently observed in running. Thus, it appears important to attempt to address some of these questions with the use of oral carbohydrates combined with non-invasive methods such as surface electromyography and transcranial magnetic stimulation of the motor cortex.

In summary, Chambers et al. (2009) show an unexpected pathway exists to counteract central fatigue development. Although central fatigue is difficult to quantify, this pioneer study again underlines the fact that the brain must always be considered when studying fatigue. Further studies are needed to extend these data and identify the underlying mechanisms explaining the non-metabolic, central positive impact of oral carbohydrates in order to optimize endurance performance. Puzzled I may be, but I am also excited about the prospect of future findings.